First described in AD 160 by Galen, the esophagus has proved to be a challenging organ to understand and manipulate. Its complex physiology and treacherous location in the posterior mediastinum precluded surgical manipulation until the twentieth century. The first thoracic esophageal resection was described by Torek in 1915.¹ He illustrated a resection of the midesophagus with an extraanatomic reconstruction. Although he described only one survivor, this event heralded the beginning of esophageal surgery. For the remainder of this century and into the next, surgeons have endeavored to improve the technique and outcomes of this thoracic specialty.

Orringer and Sloan popularized a transhiatal approach to esophageal resection and a gastric tube reconstruction.² Mckeown described a three-field approach requiring a thoracotomy to perform the majority of the esophageal dissection, followed by a laparotomy for the gastric mobilization, and finally, a cervical incision for anastomosis.³ Variations in approaches and reconstructions have provided today's surgeons with a large armament of techniques and fodder for debate over the ideal approach.

Open surgical procedures remain the standard of care for esophageal resections in most medical centers. However, the morbidity and mortality associated with open procedures and the diseases for which they are required still reveal the need for further improvement. A 10-year review of the esophagectomy experience within the Veterans' Affairs hospital system revealed a morbidity of 50% and a mortality of 10%.⁴ Birkmeyer and associates, in a recent analysis of a national Medicare database, revealed that the mortality rates from esophagectomy in the United States ranged from 8% in high-volume centers to 23% in low-volume centers.⁵

The advent of laparoscopy and thoracoscopy in the 1980s opened the door to the possibility of a minimally invasive approach to esophageal surgery. Initial experience with laparoscopic Nissen fundoplications formed the basis of the early surgical experience. Collard and colleagues were the first to describe a thoracoscopic technique for esophageal dissection.⁶ Although multiple reports of laparoscopic-assisted esophagectomies followed, it was not until DePaula and colleagues published their initial experience in 1996 that a totally laparoscopic esophagectomy was documented. Although this report detailed a laparoscopic transhiatal approach,^7–9 our center and others have used primarily a combined thoracoscopic and laparoscopic approach.^10–13 The thoracoscopic approach affords better visualization of the periesophageal structures, especially near the main airways and subcarinal areas. It is also less affected by patient height and body habitus and, in our experience, improves nodal dissection and overall visualization compared with the totally laparoscopic method. In 2000, Nyugen and colleagues compared the minimally invasive approach with open transthoracic and transhiatal esophagectomy.¹⁴ The minimally invasive approach documented shorter operative times, less blood loss, and shorter stays in the intensive care unit with no increase in morbidity compared with the open approach.

INDICATIONS

Indications for the minimally invasive approach for esophagectomy include Barrett's esophagus with high-grade dysplasia, end-stage achalasia, esophageal strictures, and esophageal cancer.^15–19 While most T₄ esophageal cancers generally are not amenable to any surgical approach, all other T stages should be amenable to minimally invasive esophagectomy in experienced hands. Downstaged cancer with neoadjuvant chemoradiation is also potentially resectable by a minimally invasive approach. Previous thoracic and abdominal surgery is not necessarily a contraindication depending on the extent of the previous surgery and the experience of the surgeon.

TECHNIQUE

Positioning

Esophagogastroscopy is performed in all patients to confirm the location of the tumor and the suitability of the stomach for tubularization to reach the cervical area. Tumors with significant gastric extension, if deemed resectable, generally are approached through an open laparotomy. For midesophageal tumors, a bronchoscopy is also indicated. The patient is intubated with a double-lumen endotracheal tube. Right lung isolation is necessary for adequate visualization and mobilization of the esophagus. The patient is placed in the left lateral decubitus position. Once tube position is confirmed, the right lung should be isolated immediately to provide adequate time for decompression. The position of the right scapula is marked. The operating table is flexed to move the iliac crest away from the costal margin and to expand the intercostal spaces.

Thoracoscopy

Four ports are used to access the right chest (Fig. 13-1). A 10-mm camera port is inserted in the anterior axillary line at the eighth interspace. An additional 10-mm port is placed approximately 2 cm posterior to the posterior axillary line in the eighth or ninth interspace. This is the main dissection port for the ultrasonic coagulation shears (US Surgical, Norwalk, CT). A 10-mm port is placed in the fourth interspace along the anterior axillary line. A fan retractor is placed through this port to provide retraction of the lung. Finally, a 5-mm port is placed below the scapular tip. Additionally, an endostitch is placed in the central tendon of the right diaphragm and brought out percutaneously through the lower chest wall near the costal margin using the Endo-Close device (US Surgical, Norwalk, CT). Downward traction on this stitch pulls the diaphragm inferiorly and allows better visualization of the lower esophagus and hiatus.

Dissection is begun by taking down the inferior pulmonary ligament (Fig. 13-2). The mediastinal pleura is dissected anteriorly along the plane between the edge of the lung and the esophagus and is resected with the specimen up to the azygos vein. The subcarinal lymph nodes are taken en bloc with the esophagus. Care is exercised to avoid injury to the posterior membrane of the right main stem bronchus, carina, and trachea. Dissection is carried up to the azygos vein, and the vein is divided with an Endo-GIA stapler (US Surgical, Norwalk, CT).

The mediastinal pleura is also divided inferiorly near the hiatus (see Fig. 13-2). A Penrose drain is placed around the inferior esophagus. This drain is used to provide retraction away from the posterior esophageal attachments and permit circumferential dissection along the esophagus. Tributaries from the thoracic duct to the esophagus are at risk for subsequent leak. Liberal use of endoclips here will minimize the chances of a postoperative chylous leak. Aortoesophageal attachments are also isolated, clipped, and divided. All surrounding soft tissue is taken with the esophagus, including the lymph node packets. Once the dissection is carried up to the divided azygos vein, the vagus nerve is divided, and the dissection is now performed close to the esophagus. By dissecting the surrounding tissue away from the esophagus, traction on the vagus nerve is minimized, and the risk of recurrent nerve injury is decreased. Care is taken to preserve the mediastinal pleura above the azygos vein. This precaution is an aid to maintaining the gastric tube in the mediastinum and seals the surrounding tissue to minimize leakage of any cervical drainage into the chest. The Penrose drain is moved up to the thoracic inlet to facilitate retrieval of the cervical esophagus during the neck dissection. Intercostal bupivacaine is injected to provide regional anesthesia. The lung is inflated to check for an injury to the posterior membranes of the trachea or bronchus. A 28F straight chest tube is placed through the camera port while the other ports are closed with Vicryl sutures. In general, we strive to keep the thoracoscopy time under 2 hours. Of note, however, adequate periesophageal dissection well into the thoracic inlet and low dissection toward the diaphragmatic crura will decrease the time spent in the neck and abdomen.

Laparoscopy

The patient is placed supine. The double-lumen endotracheal tube is replaced with a single-lumen tube. Five ports are used for the gastric mobilization (Fig. 13-3). A 10-mm port is placed right of midline in the epigastrium, slightly below the midpoint between the xiphoid process and the umbilicus. The port is inserted under direct vision. The patient is placed in a steep reverse Trendelenburg position. A 5-mm port is placed to the left of midline at the same level as the original port. A 5-mm, 30-degree camera is placed through this port. Additional 5-mm ports are placed at the left subcostal margin and the right subcostal margin. A 5-mm port is placed in the right flank to support a liver retractor. A self-retaining retractor is used to elevate the left lobe of the liver and expose the hiatus (Fig. 13-4). The gastrohepatic ligament is divided to expose the right crus. The gastroesophageal junction is freed from the hiatus by dissection up the right crus. The phrenoesophageal ligament is taken down, and the dissection is extended to the left crus. The right gastroepiploic arcade is identified, and the gastrocolic ligament is divided lateral to this arcade. Dissection is carried up along the greater curvature of the stomach, taking down the short gastric arteries. Once dissection is carried up toward the left crus, the posterior attachments of the gastroesophageal junction can be divided. The stomach is retracted superiorly and to the right to expose the celiac vessels. Celiac and gastric nodal tissue is dissected free and left with the specimen. The left gastric artery then is isolated and divided at the base using an Endo-GIA vascular stapler (US Surgical, Norwalk, CT). The stomach itself must be handled with care at all times to minimize any traumatic injuries to the tissue.

After the stomach is mobilized, a pyloroplasty is performed in Heinecke-Mikulicz fashion. An endostitch is placed superiorly and inferiorly on the pylorus to provide retraction (Fig. 13-5A ). Ultrasonic shears are used to incise the pylorus, and the opening is closed transversely using 2–0 interrupted endosutures (Fig. 13-5B ). A Kocher maneuver is performed, and the retrogastric and duodenal attachments are carefully dissected to achieve adequate mobilization of the gastric tube. Adequate mobilization should permit the pylorus to reach the right crus with ease. This should be reassessed at several time points during the mobilization to inform the surgeon of the degree of dissection required. If there is any difficulty with this maneuver, further pyloroantral mobilization generally is required.

The gastric tube construction is now initiated by firing the Endo-GIA stapler across the lesser-curve vessels and fat at an angle toward the incisura. For the first firing, we generally use a vascular load (white) with a staple height of 2.5 mm to minimize small-vessel oozing along the lesser curve (Fig. 13-6A ). The right gastric vessels are preserved. The angle of the first few staple firings will determine the gastric tube diameter, and the staples should be placed accordingly. We prefer to create a relatively narrow gastric tube that is approximately 4–5 cm wide. In addition, we apply slight caudal and simultaneous cephalad traction during application of the stapler to keep the gastric tube on slight stretch (Fig. 13-6B ). This will afford better length of the final tube. Subsequent firings of the stapler should be maintained in a line parallel to the greater-curvature arcade to create a consistent tube width and avoid spiraling of the tubularized gastric conduit. The staple load used along the thick gastric antrum may require the green stapling cartridge (4.8-mm height). As the stapling continues toward the fundus, we generally use the blue loads (3.5-mm height). The staple line is inspected for hemostasis. Two endosutures are used to attach the resected specimen to the gastric tube (Fig. 13-7). These sutures should be placed from the tip of the fundic portion of the tube to the lesser-curve portion of the resected specimen. This technique tends to minimize the bulk as the specimen and gastric tube are passed through the hiatus and out through the neck incision (Fig. 13-8).

Feeding Jejunostomy

An additional 10-mm port is placed in the right lower quadrant to facilitate jejunostomy tube placement. The transverse colon is retracted cephalad using a grasper applied to the adjacent fatty epiploicae, and the ligament of Treitz is identified. Approximately 40 cm from the ligament of Treitz, a loop of jejunum is attached to the anterior abdominal wall in the left lower quadrant using an endostitch. A 5F needle catheter feeding jejunostomy tube is inserted into the jejunum percutaneously using the Seldinger technique (Compat Biosystems, Minneapolis, MN). The guidewire is threaded into the small bowel, followed by the catheter, to a distance of approximately 20 cm. The jejunum is further tacked to the anterior abdominal wall using three additional endosutures as well as a single suture approximately 3 cm distal to the entrance site to prevent torsion. The feeding catheter is secured on the skin, and 10 mL of air is injected rapidly into the small bowel to test for patency and confirm intraluminal placement. If any doubts exist as to true luminal placement, an on-the-table Gastrografin study of the jejunostomy tube should be performed.

Cervical Anastomosis

A horizontal incision is made along a cervical crease above the sternal notch and extending to the left. Dissection is carried down, and platysmal flaps are developed. Dissection is continued along the anterior border of the sternocleidomastoid muscle. The omohyoid muscle is divided, and gentle dissection is continued down to the prevertebral fascia. The cervical esophagus is gently retracted medially with a peanut dissector, and careful dissection performed inferiorly should open into the thoracic inlet. The Penrose drain left in the thoracic inlet at the end of the thoracoscopic part of the surgery should be readily encountered in the neck and retracted out through the cervical wound. Once the cervical esophagus is bluntly dissected free, delivery of the specimen out the neck incision along with the attached gastric conduit is possible. An assistant observes the orientation of the gastric tube with the laparoscope as it is guided up through the hiatus. Care must be taken to preserve proper orientation and prevent spiraling or tension at the hiatus. Once the gastric tube is delivered into the neck, the two endosutures are divided. The proximal gastric tube is assessed for viability. The proximal cervical esophagus is mobilized. An auto-purse-string device (US Surgical, Norwalk, CT) is applied 2–3 cm distal to the cricopharyngeus, and the esophagus is divided. A 25-mm end-to-end anastomosis (EEA) stapler is used to perform the anastomosis. The anvil is placed in the cervical esophagus, and the purse-string is tied. The proximal gastric tube tip is opened, and the EEA stapler is inserted and directed posteriorly between the staple line and the line of the short gastric arteries. Generally, there is enough length of the gastric tube to permit the anvil to exit the gastric tube 6–8 cm distal. Once the anastomosis is complete, a nasogastric tube is guided under direct vision. The gastrotomy opening is closed by stapling off the distal 5–6 cm of the proximal gastric tube with an Endo-GIA stapler.

Attention is directed back into the abdomen. Graspers are applied to the antral area, and gentle downward traction is applied until the cervical anastomosis dips into the neck incision. This maneuver ensures the absence of redundant gastric tube above the hiatus that may have been pulled up during creation of the neck anastomosis. The gastric tube is tacked to the hiatus to prevent future herniation (Fig. 13-9). Care must be taken to avoid injuring the vascular supply. We generally apply three sutures, one from the greater-curve side to the left crus, one from the lesser-curve side to the right crus, and one on the anterior gastric tube to the central edge of the diaphragmatic hiatus. The cervical anastomosis is irrigated, and the skin is only loosely approximated with one or two staples. In our experience, multilayer suture closure of the cervical incision may lead to downward tracking of an anastomotic leak, should one occur.

RESULTS

The largest reported experience with minimally invasive esophagectomy to date highlights some of the potential advantages and pitfalls of this approach.¹² In our series of 222 patients, which has increased in size to greater than 700, the operative mortality was 1.4%. Median stay in the ICU was 1 day, and total hospital length of stay was 7 days. Mean operative time was 5.1 hours. Initially, we focused on smaller tumors, but as we gained experience, T₂ and T₃N₁ tumors were included. Fifty-one percent of all patients received neoadjuvant chemotherapy, radiation therapy, or both before minimally invasive esophagectomy. With a mean follow-up of 19 months, stage-for-stage, the survival curve was comparable with that of open esophagectomy.

Nguyen and colleagues, in a smaller series of 46 patients undergoing minimally invasive esophagectomy, reported a mean operative time of 350 minutes, blood loss of 270 mL, and an overall mortality of 4.3%.²⁰ The minimally invasive approach yielded comparable, if not better, outcomes than open approaches, as reported in the literature, in terms of length of stay (16.6 days), operating room time (336 minutes), and mortality (5.5%).²¹ In another analysis of minimally invasive esophagectomy in elderly patients over the age of 75 years, there were no operative deaths in 41 patients, and overall survival in 36 patients with esophageal cancer was 81% at 20 months.²² These findings suggest that minimally invasive esophagectomy can be performed in high-risk patients who otherwise might not be considered for surgery.

COMPLICATIONS

Morbidity associated with open esophagectomy can be significant, ranging from 35% to 50% in reported studies. An analysis of our own experience and that of other minimally invasive series reveals that the absolute rate of complications is similar, but the degree of the insult to the patient appears to be less in terms of impact on mortality and length of hospital stay. A review of some of the largest series of minimally invasive esophagectomies, transhiatal esophagectomies, and transthoracic esophagectomies compared with a 10-year review of all esophagectomies performed at the Veterans' Affairs hospital system illustrates a favorable outcome in mortality, length of stay, and several major complication criteria (Table 13-1).

MIE = minimally invasive esophagectomy; THE = transhiatal esophagectomy; TTE = transthoracic esophagectomy; N/A = result not available.

Operative Complications

THORAX

Bleeding and transfusion requirements were less with the minimally invasive approach,²³ but it is important to note that even small amounts of bleeding can obscure the operative field and may require conversion to an open procedure. Hence the aortoesophageal branches must be identified and clipped. Bleeding from the azygos vein and peribronchial arteries also must be avoided. Injury to the posterior membranes of the bronchus and trachea must be carefully avoided, especially during lymph node dissection. Cautery and harmonic scalpel use in close proximity to the posterior membranous trachea or main stem bronchus can lead to tissue damage resulting in an air leak, local ischemia, herniation of the gastric conduit, and subsequent development of a tracheogastric conduit fistula.

The thoracic duct is at risk for subtle injuries leading to the development of chylothorax. Early in our initial series of 77 patients undergoing minimally invasive esophagectomy, we noted 3 patients with delayed chylothorax. This complication led us to be more cautious in this area and to use metal clips on all branches from the thoracic duct. Vocal cord paralysis resulting from injury to the recurrent laryngeal nerve is minimized by dividing the vagus nerve just above the azygos vein and dissecting it away from the esophagus. We generally do not dissect lymph nodes above this level because of the risk of injury to the recurrent laryngeal nerves and the lack of definitive evidence that lymph node clearance is essential in this location for gastroesophageal junction tumors.

ABDOMEN

Disruption of the epiploic arcade can be devastating to the viability of the gastric tube. Likewise, one must make sure that there is adequate room at the hiatus for the conduit to lie without strangulation. In our series, the incidence of gastric tip necrosis was 3.2%. Although this is slightly higher than the rate reported by Orringer or Swanson, it was mostly associated with use of a narrow 3-cm gastric tube, which has since been abandoned for a more generous 4- to 5-cm tube. Furthermore, the overall mortality in this cohort of 222 patients was 1.4%, which is significantly lower than most open series.

Delayed hiatal herniation of abdominal viscera also can occur if the gastric conduit is not properly tacked to the hiatus. We have observed four delayed hiatal hernias in our series. All were repaired successfully. Orringer's series identified a 3% rate of splenectomy in 1085 open transhiatal esophagectomies.²⁴ As yet, no splenectomies have been reported in the minimally invasive esophagectomy series.

Orringer's open series also reported a 3% incidence of wound infection and dehiscence.²⁴ The national Veterans' Affairs study revealed a 10.9% rate of wound infection with a 3.7% rate of wound dehiscence.⁴ When open transhiatal and transthoracic procedures were evaluated prospectively, the transhiatal approach was associated with a 5% incidence of wound dehiscence, and the transthoracic approach was associated with only 2% wound dehiscence.²⁵ Delayed incisional hernias are seldom reported but are estimated to occur in 5–10% of long-term survivors. In our minimally invasive series, only a 0.9% incidence of minor wound infection was seen with one early port hernia, and no wound dehiscences were observed.¹²

Postoperative Complications

The postoperative complications observed after minimally invasive esophagectomy generally are comparable with those of an open procedure. Our overall cervical anastomotic leak rate was 11%. Of note, the anastomotic leak rate increased to 26% in a subset of 56 patients in whom a very narrow diameter (3-cm) gastric tube was constructed. However, in the other 166 patients, we constructed a 5-cm gastric conduit and observed a leak rate of only 6%.²⁶ The reported leak rate for open procedures is approximately 9.1%.²¹

The most common cardiopulmonary complications encountered in our series included atrial fibrillation (11.7%), pleural effusion (6.3%), and pneumonia (7.7%). Delayed gastric emptying was seen in only 1.8% of patients, and only 4% of patients complained of recalcitrant long-term postoperative reflux symptoms.¹² Moderate strictures at the gastroesophageal cervical anastomosis are common and generally can be managed with one or two outpatient dilations.

ALTERNATIVE APPROACHES

Minimally invasive esophagectomy encompasses an array of thoracoscopic and laparoscopic techniques that all seek to reduce the morbidity of an open procedure. Clearly, our institution favors the thoracoscopic/laparoscopic approach with a cervical anastomosis. Several other groups have reported variations in technique that may provide insight in this emerging field. Bonavina and colleagues described the use of a laparoscopic transhiatal approach with a video mediastinoscope from the cervical incision to assist their mediastinal dissection. They reported 10 of 12 successful operations with a mean operative time of 270 minutes.²⁷Mean hospital stay was 10 days with no ICU stays. Jobe and colleagues used a nasogastric tube to invert the esophagus to assist the laparoscopic transhiatal dissection.²⁸ Nguyen and colleagues²⁹ and Costi and colleagues³⁰describe approaches with an intrathoracic anastomosis. Finally, Horgan and colleagues³¹ described the use of robotics to assist in transhiatal esophagectomy. Horgan's group published a single case report on one patient who underwent a robotic dissection of the esophagus with a laparoscopic gastric mobilization and an open cervical anastomosis.

CONCLUSION

Minimally invasive esophagectomy is a technically challenging operation. Recent reports clearly demonstrate comparable, if not improved, mortality and morbidity following minimally invasive esophagectomy in centers with significant experience in open and minimally invasive techniques. Currently, an intergroup trial (ECOG 2202) is under way to assess the outcomes of minimally invasive esophagectomy in a multicenter trial setting.

EDITOR'S COMMENT

This chapter, written by the leaders in this field, not only in the US but also worldwide, is a key resource for any new esophageal surgeon. Great detail is given related to setup and execution of this difficult procedure. I have found that a firm background in laparoscopic staging and laparoscopic antireflux surgery is good preparation for becoming adept at this procedure. Unlike the authors, I do not think it is appropriate for all patients, especially those who undergo neoadjuvant chemotherapy or radiation therapy. The risks of adhesions leading to airway injury or bleeding are excessive. Likewise, I believe that unless a reasonable OR time can be achieved, it is not worth pursuing this technique for the occasional laparoscopic surgeon.

–MJK

REFERENCES